Our objective is to analyze at the synaptic level how sensory and motor representations of learned vocalizations propagate and are transformed in basal ganglia pathways of the songbird. The songbird is an essential model for exploring auditory-vocal interactions akin to those underlying human speech, because birdsong and speech require auditory feedback and involve basal ganglia pathways. The songbird brain contains a well-defined circuit for singing and song learning, including a basal ganglia pathway essential to audition-dependent song plasticity and perception. An anatomically dedicated and electrophysiological identifiable pool of neurons in the pallial nucleus HVC (HVCx neurons) is the putative source of song-related auditory and motor activity in the basal ganglia pathway. Here we seek to explore how HVCx neurons synaptically signal their basal ganglia targets during singing and auditory presentation of the same song. This proposal's overarching goals are to test in adult songbirds whether: 1) inhibition onto HVCX neurons disinhibits the output of the basal ganglia pathway, 2) HVCx cells transmit temporally similar patterns of activity during singing and song playback, and 3) altered sensory feedback disrupts this sensory-motor similarity. The clinical significance of this proposal is two-fold. First, by using intracellular recordings in the anesthetized bird and extracellular recordings from identified neurons in the freely behaving animal, the proposed experiments will provide unusual insight into synaptic processing of behaviorally salient patterns of activity in basal ganglia pathways. Second, an increasing body of research including an analysis of heritable dyspraxias, stuttering, spontaneous vocalization in Tourette's syndrome and dysarthria in Parkinson's disease, points to an important role for the basal ganglia in human speech. Therefore, this research will illuminate generalized aspects of sensorimotor processing in the basal ganglia, while revealing specialized aspects of auditory-vocal processing in basal ganglia pathways important to vocal learning and maintenance.